Nine college football players' deaths have been tied to complications of sickle cell trait since 2000.

Rachel George| Orlando Sentinel

As a young graduate assistant at Florida State, Terry Bowden remembers what defensive line/linebackers coach Chuck Amato used to tell players before the Seminoles' infamous mat drills.

"Just remember, gentlemen, the body is a wonderful machine. You will pass out before you die."

That hard-nosed mentality was shared by almost everybody on the team, and Bowden said Amato was no different than most other tough coaches who tried to instill that same quality in their players.

Now, nearly 30 years after he got his coaching start on his father Bobby's staff, Bowden cringes at what he didn't know.

Since then, his father has had a player die. In 2001, FSU linebacker Devaughn Darling collapsed in Tallahassee while participating in those offseason mat drills. Darling's death was later attributed to complications from sickle cell trait, a condition in which red blood cells collapse from their normal round shape and sickle during extreme duress. The warped blood cells become crescent-shaped, sticky and can block blood flow, sometimes causing major organ damage and even death.

Darling is one of nine college football players whose deaths have been tied to sickle cell trait since 2000. That almost all those deaths have come in the offseason is baffling to Terry Bowden and many others.

"We're not training our players to run marathons or enter mortal combat," said Bowden, now the coach at Division II North Alabama. "We're supposed to be getting them ready to play a football game."

Overwhelmingly in the past 11 years, more non-traumatic football deaths have occurred from complications from sickle cell trait than any other cause. It has accounted for nine of the 21 non-traumatic deaths in that time despite the trait existing in just 8 percent of African-Americans. It accounts for an even lesser extent in Hispanics, Caucasians and other ethnicities. And while the trait has been linked to deaths in other sports and at other levels, it has affected a much greater number of college football players.

Those deaths have many in football, athletic training and the medical community wondering what factors turn a generally benign trait into a dangerous, and sometimes fatal, medical condition.

And what role, if any, does football culture play in pushing players past their limits?

Workouts scrutinized

The nine deaths related to sickle cell trait make up approximately 42.9 percent of the 21 non-traumatic deaths in college football since 2000, a higher percentage than both heatstroke (28.6 percent) and cardiac issues (19 percent).

Of the 21 deaths, only two came during the football season. Aaron Richardson died in Sept. 2004 on the first day he walked on the team at Bowling Green. Dale Lloyd II died in Sept. 2006 running a conditioning drill the day after a 55-7 Rice loss at Florida State.

Of the other seven, two each happened in February and July and one each in March, May and August.

"None of them have been playing or practicing football. That's an alarming stat to me," said Chris Gillespie, the director of Athletic Training Education at Samford University. Gillespie was a long-time athletic trainer at the school and made changes to Samford's conditioning program after a player survived a sickling episode in the early 1990s.

"That tells me what we're doing in conditioning is what we need to look at," he said.

Most doctors and athletic trainers agree that certain factors that can make offseason conditioning drills dangerous for any player, can be especially risky for those with sickle cell trait.

These factors include:

-- First-day conditioning. Athletes might return from spring or summer break out of shape, making first-day tests more difficult. At least five of the nine deaths occurred on the first day of a training program.

A consensus statement from the National Athletic Trainers Association says athletes with sickle cell trait should "build up slowly in training with paced progressions, allowing longer periods of rest and recover between repetitions."

Many doctors and athletic trainers interviewed for this article reiterated that all athletes should be eased into a conditioning program.

A newness to college conditioning seems to be related. Three of the deceased players were freshmen, and two more were new to their teams. Ja'Quayvin Smalls died during his first workout at Western Carolina in July 2009, while Bennie Abram died at Ole Miss in Feb. 2010 in his first workout as a walk-on.

-- Maximum-effort drills. Athletic trainers say explosive activities like sprints can cause sickling within as little as two to three minutes.

"It seems like a relatively short period of time, but in general, two or three or four or five minutes of all-out effort can get these kids in trouble," said Dr. Fred H. Brennan, Jr., head team physician at New Hampshire.

-- Heat, humidity and dehydration. Six football players have died from heat-related illness or heatstroke in the past 11 years, and doctors say it can contribute to sickling episodes. An increase in body temperature that pathologists look for to confirm heat illness as a cause of death were not seen in the nine deaths of players with sickle cell trait, however.

Experts said dehydration plays a role as well.

"When these kids get dry, a little behind if you will, on their fluid balance, that seems to put them at risk," Brennan said.

-- Pre-existing illness. Ron Courson, Georgia's director of sports medicine, said even a low-grade fever is enough to consider holding a player with sickle cell trait out of a drill because of the risk of complications.

-- Altitude. The first known death related to sickle cell trait in college football came in 1974 when Polie Poitier, a native of Coral Gables, collapsed after running 800 meters in a practice at Colorado.

"At the extremes of human endurance with high humidity, high temperatures, dehydration, severe physical activity… these are physical conditions that would cause anybody to have problems. It just happens quicker, and maybe more severe, in those with sickle cell trait," said Dr. James R. Eckman, an expert on sickle cell trait and professor of medicine at Emory University.

Another similarity between some of the players who have died remains unexplained. Five played in the defensive secondary and another — UCF receiver Ereck Plancher — played a similar position on offense. All were listed between 5-foot-9 and 5-foot-11 and between 181 and 190 pounds.

While none of the doctors or athletic trainers had an explanation for those shared characteristics, a couple offered guesses.

Said Dr. Bruce L. Mitchell, an assistant professor of medicine and internist at Emory University Hospital: "A guy who is 300 pounds and playing guard or tackle is given some latitude as to how much to push himself. He's not trying to be the fastest guy on the field. He's not expected to be the fastest guy on the field. That particular guy might tend to stop, rest, pull up faster."

A former safety at New Hampshire himself, Brennan said, "Maybe some of these more skilled positions, they realize that there's a lot expected of them and they are more explosive in their ability to maximally exert themselves and maybe sustain it longer."

In short, they were able to push themselves to keep exercising after their bodies told them to stop.

Anecdotally, one other factor remains — that sickle cell trait deaths have occurred more often in college football than in other sports and even other levels of football.

Culture of toughness

Even a decade after winning a national championship at Miami, former defensive lineman Matt Walters speaks with pride about getting through the Hurricanes' offseason drills. Now an endurance athlete, Walters describes workouts that NFL players struggled with when they returned to campus.

"I know down at the University of Miami, to tell you the truth, I'd rather play a double overtime game than do one of those workouts," he said. "We looked forward to two-a-days.

"It was easier than our offseason workouts."

Walters is not alone. Many former players contacted for this article described how making it through the offseason made them better players and helped develop camaraderie with their teammates.

But the number of non-traumatic deaths, specifically in those players with sickle cell trait, has some questioning whether the toughness those workouts try to instill is coming at too high a cost.

A study led by Dr. Kevin M. Harris, director of the echocardiography laboratory at the Minneapolis Heart Institute, found that while deaths related to sickle cell trait are rare, they occur mostly in football.

The study, which is currently under peer review, examined 2,387 deaths in the 30-year U.S. National Registry of Sudden Death in Athletes and found 22 athletes had sickle cell trait. It was considered the primary cause of death in 15 cases.

While football accounted for 29 percent of total cases in the registry, it accounted for 82 percent of the deaths related to sickle cell trait. Of those 22 cases, 18 occurred during a football activity, three in basketball and one in track. College athletes accounted for 17 cases while there were four in high school and one younger than that.

"You won't find any science to figure that out," said Dr. Christopher McGrew, a team physician for New Mexico. "Basically, the bottom line is, we don't know why but there is circumstantial evidence to implicate that all these things seem to happen in football.

"That's the common denominator. Why is that?"

Some blame a culture that pushes for toughness, one where players run for punishment and athletic trainers might be intimidated by millionaire head coaches who aren't educated on the risks associated with sickle cell trait. It's an environment that prompts coaches to push their players and for players to do the same to themselves and their teammates.

"Coaches don't want to be considered soft," said Bowden, the coach at North Alabama. "The most negative thing your could write about a football team, and writers do this all the time, they're soft, they're not very tough. And that's the most negative thing you can say about a coach, to him personally, is his kids are soft."

But if that's true of coaches at all levels, why do most of the deaths seem to come on college campuses?

Former collegiate players speculated that it doesn't happen in the pros because it's a business.

"You have athletes that get paid more than the coaches, so what are you going to tell the athletes?" said former Florida defensive end Thaddeus Bullard, adding that players are more responsible and accountable for their own conditioning in the NFL.

Added Walters, "In college, you're 18 to 22 years old, you think you're tougher than you are, you don't know when to stop pushing yourself."

Part of it is also a numbers game. Rosters in the NFL are half the size of most college football programs meaning fewer athletes have a chance to have a sickling episode. But that fails to explain the high school level, where more than 1.1 million players put on pads last season, 17 times more than in college. There have been only three known sickle cell trait related deaths at that level since 2000.

Scott Galloway, head athletic trainer for DeSoto Independent School District outside of Dallas, offered two explanations. Galloway has become one of the leading experts at the high school level since Kourtni Livingston, a 14-year-old basketball player, died from complications of sickle cell trait after running a timed mile on the first day of practice in Aug. 2002.

Some, Galloway suspects, were misreported at the time of death. With a still growing awareness in the medical community, he and some other athletic trainers wonder if previous sickle cell trait related deaths were wrongly believed to have been caused by heat or heart issues — although some say that might be the case at other levels as well.

More to the point, though, the biggest difference is that even the top high school programs are not as intense as the conditioning that goes on at most NCAA Division I schools. High school coaches have to create conditioning programs that accommodate a wider spectrum of athletes.

"I think our coaches would continue to push them if they would continue to work," said Galloway. "But I think there is a point with the competitiveness of the athlete too where I think they shut it down."

The sheer number of college football players also might help explain why there are more deaths in football. Easily the largest sport, Division I football teams averaged 110.6 players on a roster last season while men's lacrosse came in second with 46.3.

With year-round practices increasing the number of participation opportunities where a player could get hurt, or die, some said college football is bound to get a black eye.

"You've got 12 basketball players, you've got 115 football players on average at most Division I schools," said Bullard. "So you take that number, and I'm sure one kid from the basketball team may possibly have it where 15, 20 kids possibly have it on the football team. So those numbers are going to be possibly skewed."

Where is the line?

The toughness football coaches seek to instill isn't new. Former Georgia coach Vince Dooley remembers not being allowed to have water until after he showered. As a player, Terry Bowden remembers staying on the field until lightning struck too close.

Coaches speak of knowing how hard they can push their players. Players said that's how they improve, that all Division I athletes who strive for success do the same.

But deaths raise the question of where that line is, and why it gets crossed.

"I don't know that you always know, but you'd better have a good medical team to do everything possibly you can do," said Dooley, who coached at Georgia for 25 years. "When they're cleared, you have to do what you do as a coach."

Added LSU coach Les Miles, "There is a fine line, but that fine line is crossed when a player says he needs to stop and the coach says anything else other than, 'You're right. You need to stop.'"

Gene Egdorf, a Houston attorney for The Lanier Law Firm, remembers his junior high coach telling players they were running until they puked. That mentality hasn't changed, as Egdorf has found representing the families of two of the nine deceased players in civil lawsuits.

Egdorf won an undisclosed settlement with Rice after Lloyd's death, with part of the agreement that Rice would help get NCAA legislation passed to test Division I athletes for sickle cell trait. Schools began mandatory testing in all sports this past academic year.

And while Egdorf said Rice officials did all of the right things after Lloyd's death, it was what led to it that has him convinced football culture is part of the problem.

Lloyd was 19 when he died after running 16 100-yard sprints on Sept. 24, 2006. It was the day after a 48-point loss at Florida State.

"If a player tells you he has a problem, there has to be a little bit of faith and trust that maybe that player really does have a problem, he's not slacking off," said Egdorf. "If Dale Lloyd is 30 yards behind the offensive linemen running sprints and he's a secondary player, something's not right. That's a lot more than goofing off."

He currently represents the family of Bennie Abram, a 20-year-old walk-on who died at Ole Miss in Feb. 2010.

"Ole Miss, it's the first practice of the offseason," Egdorf said. "I think there's that element of we're going to show you who's boss."

Trainers on watch

Often the responsibility of pulling a player from a workout falls to athletic trainers. While coaches joined them in saying athletic trainers have the final say in medical decisions, some veteran athletic trainers admitted it can be intimidating saying no to a coach who wants a player to finish a drill.

"It can be, but the bottom line is that's your job," said Courson, who has been at Georgia for 17 years. "I don't work for my football coach. I work with my football coach."

Many athletic trainers have suggested changes to conditioning programs, while keeping players with sickle cell trait on a watch list during intense workouts as they would for players with asthma or diabetes.

The rising number of deaths has some questioning whether offseason drills make sense for football or whether their sole purpose is to toughen players up. Bowden asked that in a piece for Yahoo! Sports in 2008 when he was a college football analyst. Courson echoed the sentiment.

"I think you've got to take a critical look at what you're doing and does it make sense?" Courson said. "With the conditioning drills you're doing, are they conditioned for football?"

In a 2010 editorial for the American College of Sports Medicine, McGrew calculated that a standard game contains 11 to 12 minutes of action, with plays lasting four to eight seconds and anywhere from 15 to 55 seconds between plays. He argued that drills should reflect that.

"Conditioning sessions and preseason drills associated with death of a player seem to have a common theme: too much, too fast, too soon, and too long," McGrew wrote.

Many experts said while athletes with sickle cell trait should be monitored more closely, the takeaway is this — no athletes should be exercised to the point that they are at a significantly higher risk of dying. If that doesn't happen, the chance of sickle cell trait becoming a factor is greatly decreased.

"You treat everybody the same," said Brennan, "with the idea of being smart and not putting everybody under extreme conditions."

Army made changes

It is the military, an institution slow to change, that some experts now point to as the model for how college football can better handle athletes with sickle cell trait.

The Army first noticed sickling in basic training recruits in 1968 and studied it extensively in the 1970s and 1980s. A review by Army physicians found those with sickle cell trait 30 to 40 times more likely to die during basic training.

Instead of testing everyone for the trait, the military made changes to basic training to make it safer for all recruits. The military's new guidelines weren't In place in 1975 when Mitchell was going through Navy basic training in Orlando. Now an internist and professor of medicine at Emory, Mitchell remembers passing out several times.

It wasn't until he became a Naval medic that he learned he has sickle cell trait, and he has devoted much of his more than 20-year career to researching it. That several players have died from what Mitchell, and many others, think to be mostly preventable causes speaks to the demands of college football.

"In the military, you march around with a rifle and you might have some calisthenics and you stop, but the level of intensity doesn't compare," he said. "Unless you're going through Seal training or something like that.

"The college athletics workout and push to improve stamina and conditioning, to me, is way more than the military."

Those who have gone through the intense offseason workouts defend them. Bullard has sickle cell trait and praised coaches and trainers who he said helped make him better. Walters agreed, and so did many others interviewed for this article.

"I think they were very difficult. We trained ourselves to be the best that we could be," said former Florida center Mike Pouncey. "You see that guys push themselves to their limit, basically. You know those guys are going to be in the game with you."

Many others said a football culture that promotes that kind of toughness for toughness' sake deserves a second look in addressing deaths related to sickle cell trait. While doctors and athletic trainers said they've made strides in educating their coaches on the risks, they hope these nine cases can help emphasize the importance of education and safe offseason conditioning drills.

"It may not be completely 100 percent preventable, just like that accident on the field when somebody gets hit might not be completely 100 percent preventable," said Gillespie. "But if you tell a kid, 'Don't drop your head and hit with the top of your head,' why can't we tell a kid, 'OK, you need to rest'?"